Comparison of size-structured and species-level trophic networks reveals antagonistic effects of temperature on vertical trophic diversity at the population and species level

It is predicted that warmer conditions should lead to a loss of trophic levels, as larger bodied consumers, which occupy higher trophic levels, experience higher metabolic costs at high temperature. Yet, it is unclear whether this prediction is consistent with the effect of warming on the trophic structure of natural systems. Furthermore, effects of temperature at the species level, which arise through a change in species composition, may differ from those at the population level, which arise through a change in population structure. We investigate this by building species-level trophic networks, and size-structured trophic networks, as a proxy for population structure, for 18 648 stream fish communities, from 4 145 234 individual fish samples, across 7024 stream locations in France from 1980 to 2008. We estimated effects of temperature on total trophic diversity (total number of nodes), vertical trophic diversity (mean and maximum trophic level) and distribution of biomass across trophic level (correlation between trophic level and biomass) in these networks. We found a positive effect of temperature on total trophic diversity in both species- and size-structured trophic networks. We found that maximum trophic level and biomass distribution decreased in species-level and size-structured trophic networks, but the mean trophic level decreased only in size-structured trophic networks. These results show that warmer temperatures associate with a lower vertical trophic diversity in size-structured networks, and a higher one in species-level networks. This suggests that vertical trophic diversity is shaped by antagonistic effects of temperature on population structure and on species composition. Our results hence demonstrate that effects of temperature do not only differ across trophic levels, but also across levels of biological organisation, from population to species level, implying complex changes in network structure and functioning with warming.     

Trophic interactions and the relationship between species diversity and ecosystem stability

Several theoretical studies propose that biodiversity buffers ecosystem functioning against environmental fluctuations, but virtually all of these studies concern a single trophic level, the primary producers. Changes in biodiversity also affect ecosystem processes through trophic interactions. Therefore, it is important to understand how trophic interactions affect the relationship between biodiversity and the stability of ecosystem processes. Here we present two models to investigate this issue in ecosystems with two trophic levels. The first is an analytically tractable symmetrical plant-herbivore model under random environmental fluctuations, while the second is a mechanistic ecosystem model under periodic environmental fluctuations. Our analysis shows that when diversity affects net species interaction strength, species interactions--both competition among plants and plant-herbivore interactions--have a strong impact on the relationships between diversity and the temporal variability of total biomass of the various trophic levels. More intense plant competition leads to a stronger decrease or a lower increase in variability of total plant biomass, but plant-herbivore interactions always have a destabilizing effect on total plant biomass. Despite the complexity generated by trophic interactions, biodiversity should still act as biological insurance for ecosystem processes, except when mean trophic interaction strength increases strongly with diversity.     

Herbivore species richness, composition and community structure mediate predator richness effects and top-down control of herbivore biomass

Changes in predator species richness can have important consequences for ecosystem functioning at multiple trophic levels, but these effects are variable and depend on the ecological context in addition to the properties of predators themselves. Here, we report an experimental study to test how species identity, community attributes, and community structure at the herbivore level moderate the effects of predator richness on ecosystem functioning. Using mesocosms containing predatory insects and aphid prey, we independently manipulated species richness at both predator and herbivore trophic levels. Community structure was also manipulated by changing the distribution of herbivore species across two plant species. Predator species richness and herbivore species richness were found to negatively interact to influence predator biomass accumulation, an effect which is hypothesised to be due to the breakdown of functional complementarity among predators in species-rich herbivore assemblages. The strength of predator suppression of herbivore biomass decreased as herbivore species richness and distribution across host plants increased, and positive predator richness effects on herbivore biomass suppression were only observed in herbivore assemblages of relatively low productivity. In summary, the study shows that the species richness, productivity and host plant distribution of prey communities can all moderate the general influence of predators and the emergence of predator species richness effects on ecosystem functioning.     

Asymmetrical food web responses in trophic-level richness, biomass, and function following lake acidification

We tested for disproportional changes in annual and seasonal species richness and biomass among five trophic levels (phytoplankton, herbivorous, omnivorous, and carnivorous zooplankton, and fish) as well as altered trophic structure and ecosystem function following the 5-year experimental acidification of Little Rock Lake (Wisconsin, USA) from pH 6.1 to 4.7. Abiotic and biotic controls of trophic level response during acidification were also identified. Asymmetric reductions of species richness among trophic levels, separated by life stage and feeding type, were evident and changes in trophic structure were most pronounced by the end of the acidification period. Relative declines in richness of fish and zooplankton were greater than phytoplankton, which were generally unaffected, leading to a reduction of upper trophic level diversity. Each of the lower four trophic levels responded to a distinct combination of abiotic and biotic variables during acidification. pH was identified as a direct driver of change for only carnivorous zooplankton, while all other trophic levels were affected more by indirect interactions caused by acidification. Fluctuations in ecosystem function (zooplankton biomass and primary production) were also evident, with losses at all trophic levels only detected during the last year of acidification. The acidified basin displayed a tendency for greater variation in biomass for upper trophic levels relative to reference conditions implying greater unpredictability in ecosystem function. Together, these results suggest that trophic asymmetry may be an important and recurring feature of ecosystem response to anthropogenic stress.     

Effects of water-column mixing on bacteria,phytoplankton, and rotifers under different levels of herbivory in a shallow eutrophic lake

Water-column mixing is known to have a decisive impact on plankton communities. The underlying mechanisms depend on the size and depth of the water body, nutrient status and the plankton community structure, and they are well understood for shallow polymictic and deep stratified lakes. Two consecutive mixing events of similar intensity under different levels of herbivory were performed in enclosures in a shallow, but periodically stratified, eutrophic lake, in order to investigate the effects of water-column mixing on bacteria abundance, phytoplankton abundance and diversity, and rotifer abundance and fecundity. When herbivory by filter-feeding zooplankton was low, water-column mixing that provoked a substantial nutrient input into the euphotic zone led to a strong net increase of bacteria and phytoplankton biomass. Phytoplankton diversity was lower in the mixed enclosures than in the undisturbed ones because of the greater contribution of a few fast-growing species. After the second mixing event, at a high biomass of filter-feeding crustaceans, the increase of phytoplankton biomass was lower than after the first mixing, and diversity remained unchanged because enhanced growth of small fast-growing phytoplankton was prevented by zooplankton grazing. Bacterial abundance did not increase after the second mixing, when cladoceran biomass was high. Changes in rotifer fecundity indicated a transmission of the phytoplankton response to the next trophic level. Our results suggest that water-column mixing in shallow eutrophic lakes with periodic stratification has a strong effect on the plankton community via enhanced nutrient availability rather than resuspension or reduced light availability. This fuels the basis of the classic and microbial food chain via enhanced phytoplankton and bacterial growth, but the effects on biomass may be damped by high levels of herbivory. Received: 3 May 1999 / Accepted: 13 April 2000     

A general biodiversity–function relationship is mediated by trophic level

Species diversity affects the functioning of ecosystems, including the efficiency by which communities capture limited resources, produce biomass, recycle and retain biologically essential nutrients. These ecological functions ultimately support the ecosystem services upon which humanity depends. Despite hundreds of experimental tests of the effect of biodiversity on ecosystem function (BEF), it remains unclear whether diversity effects are sufficiently general that we can use a single relationship to quantitatively predict how changes in species richness alter an ecosystem function across trophic levels, ecosystems and ecological conditions. Our objective here is to determine whether a general relationship exists between biodiversity and standing biomass. We used hierarchical mixed effects models, based on a power function between species richness and biomass production (Y = a × S^b), and a database of 374 published experiments to estimate the BEF relationship (the change in biomass with the addition of species), and its associated uncertainty, in the context of environmental factors. We found that the mean relationship (b = 0.26, 95% CI: 0.16, 0.37) characterized the vast majority of observations, was robust to differences in experimental design, and was independent of the range of species richness levels considered. However, the richness–biomass relationship varied by trophic level and among ecosystems; in aquatic systems b was nearly twice as large for consumers (herbivores and detritivores) compared to primary producers; in terrestrial ecosystems, b for detritivores was negative but depended on few studies. We estimated changes in biomass expected for a range of changes in species richness, highlighting that species loss has greater implications than species gains, skewing a distribution of biomass change relative to observed species richness change. When biomass provides a good proxy for processes that underpin ecosystem services, this relationship could be used as a step in modeling the production of ecosystem services and their dependence on biodiversity.     

运用稳定同位素技术分析大宁河主要鱼类营养层级

运用氮稳定同位素技术分析了大宁河静水水域和流水河段主要鱼类的氮稳定同位素比值和营养层级,并对静水水域不同水文时期相同鱼类的营养层级进行了比较研究。结果表明, 颗粒有机物(POM)氮稳定性同位素变化幅度较大, 并存在季节差异。大宁河下游静水水域鱼类15N 值范围为4.5417.51, 营养级处于1.513.88, 平均营养层级为2.49;上游流水水域鱼类的15N 值范围为2.2510.81, 营养层级范围为1.494.01, 平均营养层级为2.87。大宁河上游鱼类的平均营养层级大于下游静水水域, 可能是由于上游底栖生物丰富, 鱼类倾向摄食适口性更高的动物性食物而导致。大宁河下游静水水域汛期的鱼类营养层级较非汛期的值显著降低, 可能是因为汛期的水文扰动影响鱼类摄食中间捕食者, 以及水位的降低导致鱼类食物竞争增加迫使其摄食低营养水平的食物。重复基准生物采样建立精确充足的基线值以及确定合适的富集度,是提高营养层级评估准确性的重要手段。       

Climate change and unequal phenological changes across four trophic levels: constraints or adaptations?

1. Climate change has been shown to affect the phenology of many organisms, but interestingly these shifts are often unequal across trophic levels, causing a mismatch between the phenology of organisms and their food. 2. We consider two alternative hypotheses: consumers are constrained to adjust sufficiently to the lower trophic level, or prey species react more strongly than their predators to reduce predation. We discuss both hypotheses with our analyses of changes in phenology across four trophic levels: tree budburst, peak biomass of herbivorous caterpillars, breeding phenology of four insectivorous bird species and an avian predator. 3. In our long-term study, we show that between 1988 and 2005, budburst advanced (not significantly) with 0.17 d yr(-1), while between 1985 and 2005 both caterpillars (0.75 d year(-1)) and the hatching date of the passerine species (range for four species: 0.36-0.50 d year(-1)) have advanced, whereas raptor hatching dates showed no trend. 4. The caterpillar peak date was closely correlated with budburst date, as were the passerine hatching dates with the peak caterpillar biomass date. In all these cases, however, the slopes were significantly less than unity, showing that the response of the consumers is weaker than that of their food. This was also true for the avian predator, for which hatching dates were not correlated with the peak availability of fledgling passerines. As a result, the match between food demand and availability deteriorated over time for both the passerines and the avian predators. 5. These results could equally well be explained by consumers' insufficient responses as a consequence of constraints in adapting to climate change, or by them trying to escape predation from a higher trophic level, or both. Selection on phenology could thus be both from matches of phenology with higher and lower levels, and quantifying these can shed new light on why some organisms do adjust their phenology to climate change, while others do not.     

The functional role of biodiversity in ecosystems: incorporating trophic complexity

Understanding how biodiversity affects functioning of ecosystems requires integrating diversity within trophic levels (horizontal diversity) and across trophic levels (vertical diversity, including food chain length and omnivory). We review theoretical and experimental progress toward this goal. Generally, experiments show that biomass and resource use increase similarly with horizontal diversity of either producers or consumers. Among prey, higher diversity often increases resistance to predation, due to increased probability of including inedible species and reduced efficiency of specialist predators confronted with diverse prey. Among predators, changing diversity can cascade to affect plant biomass, but the strength and sign of this effect depend on the degree of omnivory and prey behaviour. Horizontal and vertical diversity also interact: adding a trophic level can qualitatively change diversity effects at adjacent levels. Multitrophic interactions produce a richer variety of diversity-functioning relationships than the monotonic changes predicted for single trophic levels. This complexity depends on the degree of consumer dietary generalism, trade-offs between competitive ability and resistance to predation, intraguild predation and openness to migration. Although complementarity and selection effects occur in both animals and plants, few studies have conclusively documented the mechanisms mediating diversity effects. Understanding how biodiversity affects functioning of complex ecosystems will benefit from integrating theory and experiments with simulations and network-based approaches.     

Complex wasp-waist regulation of pelagic ecosystems in the Pacific Ocean

‘Wasp-waist’ control of marine ecosystems is driven by a combination of top-down and bottom-up forcing by a few abundant short-lived species occupying intermediate trophic levels that form a narrow ‘waist’ through which energy flow from low to high trophic levels is controlled. It has been assumed that wasp-waist control occurs primarily in highly productive and species-poor systems (e.g. upwelling regions). Two large, species-rich, pelagic ecosystems in the relatively oligotrophic eastern and western Pacific Ocean also show wasp-waist-like structure, in that short-lived and fast-growing cephalopods and fishes at intermediate trophic levels comprise the vast majority of the biomass. Possible forcing dynamics of these systems were examined using ecosystem models by altering the biomass of phytoplankton (bottom-up forcing), large pelagic predators (top-down forcing), and intermediate ‘wasp-waist’ functional groups independently and observing how these changes propagated throughout the ecosystem. The largest effects were seen when altering the biomass of mid trophic-level epipelagic and mesopelagic fishes, where dramatic trophic cascades occurred both upward and downward in the system. We conclude that the high productivity and standing biomass of animals at intermediate trophic levels has a strong top-down influence on the abundance of primary producers. Furthermore, their importance as prey for large predators results in bottom-up controls on populations at higher trophic levels. We show that these tropical pelagic ecosystems possess a complex structure whereby several waist groups and alternate trophic pathways from primary producers to apex predators can cause unpredictable effects when the biomasses of particular functional groups are altered. Such models highlight the possible structuring mechanisms in pelagic systems, which have implications for fisheries that exploit these wasp-waist groups, such as squid fisheries, as well as for fisheries of top predators such as tunas and billfishes that prey upon wasp-waist species.     

Are algal communities driven toward maximum biomass?

In this continental-scale study, we show that in major benthic and planktonic stream habitats, algal biovolume--a proxy measure of biomass--is a unimodal function of species richness (SR). The biovolume peak is observed at intermediate to high SR in the benthos but at low richness in the phytoplankton. The unimodal nature of the biomass-diversity relationship implies that a decline in algal biomass with potential harmful effects on all higher trophic levels, from invertebrates to fish, can result from either excessive species gain or species loss, both being common consequences of human-induced habitat alterations. SR frequency distributions indicate that the most frequent richness is habitat-specific and significantly higher in the benthos than in the plankton. In all studied stream environments, the most frequent SR is lower than the SR that yields the highest biovolume, probably as a result of anthropogenic influences, but always within one standard deviation from it, i.e. they are statistically indistinguishable. This suggests that algal communities may be driven toward maximum biomass.     

Reef Fishes at All Trophic Levels Respond Positively to Effective Marine Protected Areas

Marine Protected Areas (MPAs) offer a unique opportunity to test the assumption that fishing pressure affects some trophic groups more than others. Removal of larger predators through fishing is often suggested to have positive flow-on effects for some lower trophic groups, in which case protection from fishing should result in suppression of lower trophic groups as predator populations recover. We tested this by assessing differences in the trophic structure of reef fish communities associated with 79 MPAs and open-access sites worldwide, using a standardised quantitative dataset on reef fish community structure. The biomass of all major trophic groups (higher carnivores, benthic carnivores, planktivores and herbivores) was significantly greater (by 40% - 200%) in effective no-take MPAs relative to fished open-access areas. This effect was most pronounced for individuals in large size classes, but with no size class of any trophic group showing signs of depressed biomass in MPAs, as predicted from higher predator abundance. Thus, greater biomass in effective MPAs implies that exploitation on shallow rocky and coral reefs negatively affects biomass of all fish trophic groups and size classes. These direct effects of fishing on trophic structure appear stronger than any top down effects on lower trophic levels that would be imposed by intact predator populations. We propose that exploitation affects fish assemblages at all trophic levels, and that local ecosystem function is generally modified by fishing.     

The performance of models relating species geographical distributions to climate is independent of trophic level

Species–climate ‘envelope’ models are widely used to evaluate potential climate change impacts upon species and biodiversity. Previous studies have used a variety of methods to fit models making it difficult to assess relative model performance for different taxonomic groups, life forms or trophic levels. Here we use the same climatic data and modelling approach for 306 European species representing three major taxa (higher plants, insects and birds), and including species of different life form and from four trophic levels. Goodness‐of‐fit measures showed that useful models were fitted for >96% of species, and that model performance was related neither to major taxonomic group nor to trophic level. These results confirm that such climate envelope models provide the best approach currently available for evaluating reliably the potential impacts of future climate change upon biodiversity.     

Species richness changes across two trophic levels simultaneously affect prey and consumer biomass

Increasing species richness of primary producers or consumers is proposed to increase primary and secondary production; however, the consequences of biodiversity change across trophic levels has been poorly investigated. We used a controlled marine microbial system to investigate the effects of simultaneous changes in biodiversity of consumer and prey species. Consumer (ciliates) and prey (algae) richness and identity were manipulated independently in a complete factorial design. The results showed clear biodiversity effects of both consumers and prey, within and across trophic levels. We found reduced prey and increased consumer biomass with increased consumer richness, with the most diverse prey assemblage supporting the highest biomass of consumers at the highest richness of consumers. Increasing prey richness did not increase resistance to consumption when consumers were present. Instead, our results indicated enhanced energy transfer with simultaneous increasing richness of consumers and prey.     

Why are predators more sensitive to habitat size than their prey? Insights from bromeliad insect food webs

Ecologists have hypothesized that the exponent of species-area power functions (z value) should increase with trophic level. The main explanation for this pattern has been that specialist predators require prior colonization of a patch by their prey, resulting in a compounding of the effects of area up trophic levels. We propose two novel explanations, neither of which assumes trophic coupling between species. First, sampling effects can result in different z values if the abundances of species differ (in mean or evenness) between trophic levels. Second, when body size increases between trophic levels, effects of body size on z values may appear as differences between trophic levels. We test these alternative explanations using invertebrate food webs in 280 bromeliads from three countries. The z value of predators was higher than that of prey. Much of the difference in z values could be explained by sampling effects but not by body size effects. When damselflies occurred in the species pool, predator z values were even higher than predicted, as damselflies avoid small, drought-prone bromeliads. In one habitat, dwarf forests, detrital biomass became decoupled from bromeliad size, which also caused large trophic differences in z values. We argue that there are often simpler explanations than trophic coupling to explain differences in z values between trophic levels.     

The role of predation for seasonal variability patterns among phytoplankton and ciliates

Investigating the mechanisms which underlie the biomass fluctuations of populations and communities is important to better understand the processes which buffer community biomass in a variable environment. Based on long-term data of plankton biomass in Lake Constance (Bodensee), this study aims at explaining the different degree of synchrony among populations observed within two freshwater plankton groups, phytoplankton and ciliates. Established measures of temporal variability such as the variance ratio and cross-correlation coefficients were combined with first-order autoregressive models that allow estimating species interactions from time-series data. We found that predation was an important driver of the observed seasonal variability patterns in phytoplankton and ciliates, and that competitive interactions only played a subordinate role. In Lake Constance copepods and cladocerans, two major invertebrate predator groups, focus their grazing pressure at different times of the season. Model results suggested that compensatory dynamics detected in phytoplankton originate from the differential vulnerability of species to either one of these two predator groups. For ciliates model results advocated that synchrony among species occurs because ciliates tend to be vulnerable to both predator groups. Our findings underline the necessity of extending studies of community variability to multiple trophic levels because accounting for predator-prey interactions may often be more important than accounting for competitive interactions at one trophic level.     

Cascading effects of predator diversity and omnivory in a marine food web

Over‐harvesting, habitat loss and exotic invasions have altered predator diversity and composition in a variety of communities which is predicted to affect other trophic levels and ecosystem functioning. We tested this hypothesis by manipulating predator identity and diversity in outdoor mesocosms that contained five species of macroalgae and a macroinvertebrate herbivore assemblage dominated by amphipods and isopods. We used five common predators including four carnivores (crabs, shrimp, blennies and killifish) and one omnivore (pinfish). Three carnivorous predators each induced a strong trophic cascade by reducing herbivore abundance and increasing algal biomass and diversity. Surprisingly, increasing predator diversity reversed these effects on macroalgae and altered algal composition, largely due to the inclusion and performance of omnivorous fish in diverse predator assemblages. Changes in predator diversity can cascade to lower trophic levels; the exact effects, however, will be difficult to predict due to the many complex interactions that occur in diverse food webs.     

The relationship between biodiversity and ecosystem functioning in food webs

Recent theoretical and experimental work provides clear evidence that biodiversity loss can have profound impacts on functioning of natural and managed ecosystems and the ability of ecosystems to deliver ecological services to human societies. Work on simplified ecosystems in which the diversity of a single trophic level is manipulated shows that diversity can enhance ecosystem processes such as primary productivity and nutrient retention. Theory also strongly suggests that biodiversity can act as biological insurance against potential disruptions caused by environmental changes. However, these studies generally concern a single trophic level, primary producers for the most part. Changes in biodiversity also affect ecosystem functioning through trophic interactions. Here we review, through the analysis of a simple ecosystem model, several key aspects inherent in multitrophic systems that may strongly affect the relationship between diversity and ecosystem processes. Our analysis shows that trophic interactions have a strong impact on the relationships between diversity and ecosystem functioning, whether the ecosystem property considered is total biomass or temporal variability of biomass at the various trophic levels. In both cases, food-web structure and trade-offs that affect interaction strength have major effects on these relationships. Multitrophic interactions are expected to make biodiversity–ecosystem functioning relationships more complex and non-linear, in contrast to the monotonic changes predicted for simplified systems with a single trophic level.     

Woody plant phylogenetic diversity mediates bottom–up control of arthropod biomass in species-rich forests

Global change is predicted to cause non-random species loss in plant communities, with consequences for ecosystem functioning. However, beyond the simple effects of plant species richness, little is known about how plant diversity and its loss influence higher trophic levels, which are crucial to the functioning of many species-rich ecosystems. We analyzed to what extent woody plant phylogenetic diversity and species richness contribute to explaining the biomass and abundance of herbivorous and predatory arthropods in a species-rich forest in subtropical China. The biomass and abundance of leaf-chewing herbivores, and the biomass dispersion of herbivores within plots, increased with woody plant phylogenetic diversity. Woody plant species richness had much weaker effects on arthropods, but interacted with plant phylogenetic diversity to negatively affect the ratio of predator to herbivore biomass. Overall, our results point to a strong bottom–up control of functionally important herbivores mediated particularly by plant phylogenetic diversity, but do not support the general expectation that top–down predator effects increase with plant diversity. The observed effects appear to be driven primarily by increasing resource diversity rather than diversity-dependent primary productivity, as the latter did not affect arthropods. The strong effects of plant phylogenetic diversity and the overall weaker effects of plant species richness show that the diversity-dependence of ecosystem processes and interactions across trophic levels can depend fundamentally on non-random species associations. This has important implications for the regulation of ecosystem functions via trophic interaction pathways and for the way species loss may impact these pathways in species-rich forests.